Coevolution of parasites and hosts 1) Evolution of host-parasite interactions 2) Evolution of virulence 3) Trade-offs in host defense 4) Brood parasitism - an arms race? 5) End of arms race? 6) Example exam questions
Coevolution of parasites and hosts
1) Evolution of host-parasite interactions
2) Evolution of virulence
3) Trade-offs in host defense
4) Brood parasitism - an arms race?
5) End of arms race?
6) Example exam questions
Parasitism:Individuals of one species live on or in members of another species, which are not killed immediately.
One party (parasite) gains at the expense of the other (host).
Coevolution (strictly):
Reciprocal evolutionary change of interacting species
1) Evolution of host-parasite interactions
Ÿ immune systems and pathogens
Ÿ chemical and physical defenses against phytophagous insects (e.g., Heliconius caterpillars on Passiflora vines)
Ÿ brood parasitism (e.g., cuckoos and hosts)
Ÿ kleptoparasitism (e.g., frigate birds)
Ÿ interspecific “slavery” (e.g., ants)
1) Evolution of host-parasite interactions
Colony foundation by Epimyrma queens follows the typical pattern seen in many temporary social parasites and obligatory slave makers, and involves the forceful usurpation of a host colony. ... E. kraussei queens approach host colonies in an aggressive manner. Once the parasite penetrates the host nest, she kills the host queen and is adopted by the host workers.
The queens of E. ravouxi use a more 'conciliatory' approach initially, grooming and stroking host workers, but, once inside the nest, the parasite mounts the host queen from behind and kills her by seizing her around the neck with her sabre-shaped mandibles.
Interspecific slavery in ants
Photo of E. ravouxi by Olivier Delattrehttp://the-scorpion-and-the-frog.blogspot.ca/2012_10_01_archive.html
E. stumperi queens crouch down, freeze and seem to feign death during their initial encounters with host workers, but subsequently begin to mount workers from behind and to groom them, perhaps acquiring chemical recognition cues in the process. However, once inside the nest, the parasite queen systematically eliminates the host queens by mounting them, rolling them over and grasping their necks in her mandibles until they succumb.
- Lewis, et al, eds. 2002. The behavioural ecology of parasites. CABI.
1) Evolution of host-parasite interactions
The conventional wisdom once was that parasites should evolve reduced virulence to their hosts.
This was based on observations that
- some mutualistic associations have evolved from once-pathogenic interactions (lichens? mycorrhizal fungi?).
- highly virulent parasites kill their hosts, and thereby themselves.
- examples of attenuation of virulence in some disease outbreaks
2) Evolution of virulence
An alternative perspective is that selection should favor genotypes whose level of virulence maximizes their rate of increase.
Those are not necessarily the genotypes with the lowest virulence.
The optimum virulence is likely to depend on a balance between the advantages of high virulence (rapid multiplication leading to increased transmission rate) and disadvantages of high virulence (increased host mortality).
Consequently, with selection might often favor an intermediate degree of virulence.
2) Evolution of virulence
Evolution of Myxoma virulence
2) Evolution of virulence
100
150
200
250
Rabbit a
bundance
Rabbit fleas introducedMyxomatosis introduced
Recorded rabbit plagues
0
50
1927
1931
1935
1939
1943
1947
1951
1955
1959
1963
1967
1971
1975
1979
1983
1987
1991
1995
1999
2003
2007
Rabbit abundance in northeast South Australia accompanyingrapid evolution of lower virulence by viruses (and of resistance by rabbits)
Saunders et al (2010) Biol Control
Rabbit HemorrhagicDisease introduced
2) Evolution of virulence
Evolution of Myxoma virulence
2) Evolution of virulence
Parasite: barley stripe mosaic virus
Host: barley (Hordeum vulgare)
vertical transmissiontreatment
(4 barley generations,transmission by seeds)
horizontal transmission treatment (4 barley generations)
Stewart et at. (2005)
http://www.albertabarley.com/barley/barley/images/BarleyCommission-stock4.JPG
Experimental evolution of virulence2) Evolution of virulence
“virulence” measured bynumber of viable seeds produced by infected plant
Stewart et at. (2005)1 – (viable seeds of infected plants) / (viable seeds of control plants) x 100%
horizontal transmission treatment (4 barley generations)
2) Evolution of virulence
Stewart et at. (2005)
vertical transmission treatment
2) Evolution of virulence
Re
lati
ve
fre
qu
en
cy
Virulence (% deaths per infection)
Re
lati
ve
fre
qu
en
cy
0.01 0.1
0.6
0.8
0.4
0.4
0.6
0.2
0.2
0.0
0.0
Ewald (1993)
1.0 10.0 100.0
Diseases transmitted directly
Diseases transmitted byinsect vector
Virulence and mode of transmission of human diseases
2) Evolution of virulence
Ewald (1993)
Waterborne human diseases are deadly
Outb
reaks
of dis
ease
cause
d b
yw
ate
rborn
e p
ath
ogens
(% o
f to
tal)
Virulence (% of deaths per infection)
2) Evolution of virulence
Coevolution between wild parsnip and the parsnip webworm
Negative genetic correlations between leaf secondary compounds (furanocoumarins) and indices of flower size
Berenbaum et al (1986)
Cost of defense in wild parsnip
http://www.ontariowildflower.com/lakeedge.htm
3) Trade-offs in host defense
Zangerl & Berenbaum 2005
Wild parsnip was introduced to North America before the parsnip webworm. In the 1800's, concentrations of furanocoumarins in parsnip seeds in herbarium specimens were lower than that in Old World plants (indicated by horizontal bars). Furanocoumarin concentrations rose after webworm damage began to appear (1900's).
http://mothphotographersgroup.msstate.edu/larva.php?plate=01.0&sort=h© N. Schneider
Coevolution between wild parsnip and the parsnip webworm
3) Trade-offs in host defense
Coevolution between European cuckoos and hosts
reed warbler
reed warbler nest
cuckoo chick
http://fleetpond.wordpress.com/2009/05/
4) Brood parasitism - an arms race?
Adaptation: Nest parasitism by European cuckoos
Newly-hatched cuckoo chickejecting host eggs and chicks
4) Brood parasitism - an arms race?
Hosts frequently parasitized by common cuckoo in the UK are reed warbler, meadow pipit, pied wagtail, and dunnock.
Pied wagtail
Dunnock
Reed warb
ler
Meadow pipit
reject
keep
Frequency of rejection by reed warblers of rubber model cuckoo eggs placed in their nests
Type of model cuckoo egg added to nest
Num
be
r of nest
s
0
5
10
15
20
Counteradaptation: Host species have evolved rejection of eggs unlike their own
Brooke & Davies (1988)
4) Brood parasitism - an arms race?
28 5
30 22
27 5
11 23
Britaincuckoospresent
Icelandcuckoosabsent
Reject
Keep
Reject
Keep
Meadow pipit
Pied/white wagtail
Davies & Brooke (1989)
4) Brood parasitism - an arms race?Counteradaptation:
Host species have evolved rejection of eggs unlike their own
Host populations in Iceland, where cuckoos are absent, are less likely to reject eggs unlike their own than in Britain, where cuckoos are present.
robin
pied wagtail
dunnock
reed warbler
meadow pipit
host cuckoo model
Counter-counter adaptation:Cuckoos have evolved egg mimicry (or not, in case of dunnock)
4) Brood parasitism - an arms race?
Brooke & Davies (1988)
Meadow pipit
Dunnock
Reedwarbler
http://www.britannica.com/EBchecked/topic-art/128222/21/Coevolution-of-one-species-with-many-species
4) Brood parasitism - an arms race?Counter-counter adaptation:
Cuckoos have evolved egg mimicry (or not, in case of dunnock)
4) Brood parasitism - an arms race?Counter-counter adaptation:
Cuckoos have evolved egg mimicry (or not, in case of dunnock)
Stoddard & Stevens (2011) Evolution
´
Host rejection rate of nonmimetic eggs and mean “just noticeable differences” (JND - a composite metric) between cuckoo and host eggs in background color and background luminance. Data from continental Europe. Closer mimicry is associated with higher rejection rates of eggs unlike the hosts’ own.
Counter-counter adaptation:Cuckoos have evolved hawk-like ‘chuckle’ call
4) Brood parasitism - an arms race?
Pro
ba
bili
ty o
f e
gg
acc
ep
tan
ce
0.0
0.2
0.4
0.6
0.8
1.0
6/18 6/17 13/17 13/18
a b
Collareddove
Malecuckoo
Femalecuckoo
Sparrowhawk
Fig. 2 | Reed warblers were more likely to accept a foreign egg after playback of female cuckoo or hawk calls than after the calls of a male cuckoo or
dove. a, A reed warbler clutch with one egg painted brown to simulate parasitism. b, The probability of reed warblers accepting a foreign egg one day after
the experiment was greater after exposure to female cuckoo or hawk calls compared with dove or male cuckoo calls (experiment 3 in Table ; n =1 70 nests;
data are predicted means ± s.e.m.; the raw proportions of the nests in which foreign eggs were accepted are also shown at the base of each bar). Male 2cuckoo calls had no more effect than control dove calls =(χ 0.015; P = 0.90), whereas female cuckoo calls reduced egg rejection as much as hawk calls
2(χ = 0.083; P = 0.77).
York & Davies (2017) Nature Ecology & Evolution
4) Brood parasitism - an arms race?Counter-counter adaptation:
Cuckoos have evolved egg mimicry (or not, in case of dunnock)
The paradox of the dunnock - why no egg rejection?
https://www.rspb.org.uk/birds-and-wildlife/bird-and-wildlife-guides/bird-a-z/d/dunnock/
Absence of chick recognition by hosts
Rate of food provisioning to cuckoo chickscompared to other chicks
Davies et al. (1998)
Loads
bro
ught per
hour
Chick species
4) Brood parasitism - an arms race?
Davies et al. (1998)
Single reed warbler chick
Brood of 4 reed warbler chicks
One cuckoo chick
One blackbird chick
Loads
bro
ught per
hour
Begging sound played
4) Brood parasitism - an arms race?
Provisioning rate by reed warbler parents (mean + 1SE) to single blackbird (n=6) or song thrush (n=3) chicks tested with no sound, sound of cuckoo chick begging, or sound of a brood of four reed warblers.
Cuckoo chicks have evolved begging call like that of host (reed warbler)
Sonograms of begging calls (recorded 60 min after feeding to satiation)
Davies & Brooke (1989)
Some non-host species have evolved high egg rejection rates
5) End of arms race?
Percent of nests rejecting unlike model eggs
Perc
en
t of sp
eci
es
0
20
40
60
80
0 20 40 60 80 100
unsuitable hosts
suitable rare hosts
0
20
40
60
80
current hosts
Davies & Brooke (1989)
Some non-host species have evolved high egg rejection rates
Percent of nests rejecting unlike model eggs
Perc
en
t of sp
eci
es
0
20
40
60
80
0 20 40 60 80 100
unsuitable hosts
suitable rare hosts
0
20
40
60
80
current hosts
linnetgreenfinchbullfinch
chaffinch
Feed seeds to young
Feeds insects to young
5) End of arms race?
Davies & Brooke (1989)
Some non-host species have evolved high egg rejection rates
Percent of nests rejecting unlike model eggs
Perc
en
t of sp
eci
es
0
20
40
60
80
0 20 40 60 80 100
unsuitable hosts
suitable rare hosts
0
20
40
60
80
current hosts
pied flycatcher
spotted flycatcher
Nests in treeholes
Has open nest
5) End of arms race?
6) Example exam questions
Why are some parasites more virulent than others? Present a study design for testing alternative hypotheses.
Consider a coevolutionary interaction between a disease and its host. Under what circumstances might we expect natural selection to favor a low virulence of the disease? Under what circumstances might we expect natural selection to favor a high virulence of the disease? Explain.
Is the coevolution between cuckoo brood parasites and their avian hosts best described as an arms race or as steady-state coevolution (in the language of Abrams)? Explain your reasoning.
Is the coevolution between wild parsnip and the parsnip webworm best described as an arms race or as steady-state coevolution (in the language of Abrams)? Explain your reasoning.
Suggest a hypothesis for why waterborne human pathogens are often highly virulent. Explain the basis for your hypothesis, and suggest an experimental test.